All Title Author
Keywords Abstract

PLOS ONE  2012 

Does Mutualism Drive the Invasion of Two Alien Species? The Case of Solenopsis invicta and Phenacoccus solenopsis

DOI: 10.1371/journal.pone.0041856

Full-Text   Cite this paper   Add to My Lib


Although mutualism between ants and honeydew-producing hemipterans has been extensively recognized in ecosystem biology, however few attempts to test the hypothesis that mutualism between two alien species leads to the facilitation of the invasion process. To address this problem, we focus on the conditional mutualism between S. invicta and P. solenopsis by field investigations and indoor experiments. In the laboratory, ant colony growth increased significantly when ants had access to P. solenopsis and animal-based food. Honeydew produced by P. solenopsis also improved the survival of ant workers. In the field, colony density of P. solenopsis was significantly greater on plots with ants than on plots without ants. The number of mealybug mummies on plants without fire ants was almost three times that of plants with fire ants, indicating a strong effect of fire ants on mealybug survival. In addition, the presence of S. invicta successfully contributed to the spread of P. solenopsis. The quantity of honeydew consumption by S. invicta was significantly greater than that of a presumptive native ant, Tapinoma melanocephalum. When compared with the case without ant tending, mealybugs tended by ants matured earlier and their lifespan and reproduction increased. T. melanocephalum workers arrived at honeydew more quickly than S. invicta workers, while the number of foraging S. invicta workers on plants steadily increased, eventually exceeding that number of T. melanocephalum foragers. Overall, these results suggest that the conditional mutualism between S. invicta and P. solenopsis facilitates population growth and fitness of both species. S. invicta tends to acquire much more honeydew and drive away native ants, promoting their predominance. These results suggest that the higher foraging tempo of S. invicta may provide more effective protection of P. solenopsis than native ants. Thus mutualism between these two alien species may facilitate the invasion success of both species.


[1]  Brightwell RJ, Silverman J (2010) Invasive Argentine ants reduce fitness of red maple via a mutualism with an endemic coccid. Biological Invasions 12: 2051–2057.
[2]  Holway DA, Lach L, Suarez AV, Tsutsui ND, Case TJ (2002) The causes and consequences of ant invasions. Annual Review of Ecology and Systematics. pp. 181–233.
[3]  Helms KR, Vinson SB (2002) Widespread association of the invasive ant Solenopsis invicta with an invasive mealybug. Ecology 83: 2425–2438.
[4]  Lach L (2003) Invasive ants: Unwanted partners in ant-plant interactions? Annals of the Missouri Botanical Garden 90: 91–108.
[5]  Ness J, Bronstein J (2004) The effects of invasive ants on prospective ant mutualists. Biological Invasions 6: 445–461.
[6]  Way M (1963) Mutualism between ants and honeydew-producing Homoptera. Annual Review of Entomology 8: 307–344.
[7]  Beattie AJ (1985) The evolutionary ecology of ant-plant mutualisms: Cambridge Univ Pr.
[8]  Carter W (1973) Insects in relation to plant disease: Wiley Interscience, New York.
[9]  Buckley R (1987) Ant-plant-homopteran interactions. Advances in Ecological Research 16: 53–85.
[10]  Delabie JHC (2001) Trophobiosis between Formicidae and Hemiptera (Sternorrhyncha and Auchenorrhyncha): an overview. Neotropical Entomology 30: 501–516.
[11]  Bluthgen N, Verhaagh M, Goitia W, Jaffe K, Morawetz W, et al. (2000) How plants shape the ant community in the Amazonian rainforest canopy: the key role of extrafloral nectaries and homopteran honeydew. Oecologia 125: 229–240.
[12]  Dejean A, Corbara B (2003) A review of mosaics of dominant ants in rainforests and plantations: Cambridge University Press, Cambridge.
[13]  Vermeij GJ (1996) An agenda for invasion biology. Biological conservation 78: 3–9.
[14]  Vitousek PM, D'Antonio CM, Loope LL, Westbrooks R (1996) Biological invasions as global environmental change. American Scientist 84: 468–478.
[15]  Moller H (1996) Lessons for invasion theory from social insects. Biological conservation 78: 125–142.
[16]  Traveset A, Richardson DM (2006) Biological invasions as disruptors of plant reproductive mutualisms. Trends in Ecology & Evolution 21: 208–216.
[17]  Whittaker J (1991) Effects of ants on temperate woodland trees. Ant-plant interactions Oxford University Press, Oxford, England. pp. 67–79.
[18]  Daane KM, Sime KR, Fallon J, Cooper ML (2007) Impacts of Argentine ants on mealybugs and their natural enemies in California's coastal vineyards. Ecological Entomology 32: 583–596.
[19]  Nixon GEJ (1951) The association of ants with aphids and coccids: Commonwealth Institute of Entomology London, United Kingdom.
[20]  Buckley R (1987) Interactions involving plants, Homoptera, and ants. Annual Review of Ecology and Systematics 18: 111–135.
[21]  Banks C, Nixon H (1958) Effects of the ant, Lasius niger L., on the feeding and excretion of the bean aphid, Aphis fabae Scop. Journal of Experimental Biology 35: 703.
[22]  Mittler T (1958) The excretion of honeydew by Tuberolachnus salignus (Gmelin) (Homoptera: Aphididae). Proceedings of the Royal Entomological Society of London Series A, General Entomology 33: 49–55.
[23]  Flatt T, Weisser WW (2000) The effects of mutualistic ants on aphid life history traits. Ecology 81: 3522–3529.
[24]  Holland JN, Ness JH, Boyle A, Bronstein JL (2005) Mutualisms as consumer–resource interactions. Ecology of Predator–Prey Interactions. pp. 17–33.
[25]  H?lldobler B, Wilson EO (1990) The ants: Harvard University Press, Cambridge, MA.
[26]  Douglas A (1993) The nutritional quality of phloem sap utilized by natural aphid populations. Ecological Entomology 18: 31–38.
[27]  Tobin JE (1994) Ants as primary consumers: diet and abundance in the Formicidae. Nourishment and evolution in insect societies 9: 279–307.
[28]  Davidson DW, Cook SC, Snelling RR (2004) Liquid-feeding performances of ants (Formicidae): ecological and evolutionary implications. Oecologia 139: 255–266.
[29]  Abbott KL, Green PT (2007) Collapse of an ant-scale mutualism in a rainforest on Christmas Island. Oikos 116: 1238–1246.
[30]  Tschinkel WR (2006) The fire ants: Belknap Press.
[31]  Williams DF, Vander Meer RK, Lofgren CS (1987) Diet-induced nonmelanized cuticle in workers of the imported fire ant Solenopsis invicta buren. Archives of insect biochemistry and physiology 4: 251–259.
[32]  Sorensen AA, Vinson S (1981) Quantitative food distribution studies within laboratory colonies of the imported fire ant, Solenopsis invicta Buren. Insectes Sociaux 28: 129–160.
[33]  Williams D, Lofgren C, Lemire A (1980) A simple diet for rearing laboratory colonies of the red imported fire ant. Journal of Economic Entomology 73: 176–177.
[34]  Porter SD (1989) Effects of diet on the growth of laboratory fire ant colonies (Hymenoptera: Formicidae). Journal of the Kansas Entomological Society. pp. 288–291.
[35]  Stradling D (1978) Food and feeding habits of ants. Production ecology of ants and termites Cambridge University Press, Cambridge, MA. pp. 81–106.
[36]  Glancey BM, Meer R, Glover A, Lofgren C, Vinson S (1981) Filtration of microparticles from liquids ingested by the red imported fire ant Solenopsis invicta Buren. Insectes Sociaux 28: 395–401.
[37]  Porter SD, Savignano DA (1990) Invasion of polygyne fire ants decimates native ants and disrupts arthropod community. Ecology 71: 2095–2106.
[38]  Kaplan I, Eubanks MD (2005) Aphids alter the community-wide impact of fire ants. Ecology 86: 1640–1649.
[39]  Zeng L, Lu YY, He XF, Zhang WQ, Liang GW (2005) Identification of red imported fire ant Solenopsis invicta to invade mainland China and infestation in Wuchuan, Guangdong. Chinese Bulletin of Entomology 42: 144–148.
[40]  Fuchs TW, Stewart JW, Minzenmayer R, Rose M (1991) 1st record of Phenacoccus solenopsis tinsley in cultivated cotton in the United States. Southwestern Entomologist 16: 215–221.
[41]  Williams D, Willink M (1992) Mealybugs of Central and South America: p.635. CAB International.
[42]  Culik MP, Gullan PJ (2005) A new pest of tomato and other records of mealybugs (Hemiptera: Pseudococcidae) from Espírito Santo, Brazil. Zootaxa 964: 1–8.
[43]  Hodgson C, Abbas G, Arif MJ, Saeed S, Karar H (2008) Phenacoccus solenopsis Tinsley (Sternorrhyncha: Coccoidea: Pseudococcidae), an invasive mealybug damaging cotton in Pakistan and India, with a discussion on seasonal morphological variation. Zootaxa. pp. 1–35.
[44]  Akintola A, Ande A (2008) First record of Phenacoccus solenopsis Tinsley (Hemiptera: Pseudococcidae) on Hibiscus rosa-sinensis in Nigeria. Agricultural Journal 3: 1–3.
[45]  Lu YY, Zeng L, Wang L, Xu YJ, Chen KW (2008) Precaution of solenopsis mealybug Phenacoccus solenopsis Tinsley. Journal of Environmental Entomology 30: 386–387.
[46]  Liu SS, De Barro P, Xu J, Luan JB, Zang LS, et al. (2007) Asymmetric mating interactions drive widespread invasion and displacement in a whitefly. Science 318: 1769.
[47]  Simberloff D, Von Holle B (1999) Positive interactions of nonindigenous species: invasional meltdown? Biological Invasions 1: 21–32.
[48]  Richardson DM, Py?ek P, Rejmánek M, Barbour MG, Panetta FD, et al. (2000) Naturalization and invasion of alien plants: concepts and definitions. Diversity and distributions 6: 93–107.
[49]  Bruno JF, Stachowicz JJ, Bertness MD (2003) Inclusion of facilitation into ecological theory. Trends in Ecology & Evolution 18: 119–125.
[50]  Lu M, Miller DR, Sun JH (2007) Cross-attraction between an exotic and a native pine bark beetle: a novel invasion mechanism? PloS one 2: e1302.
[51]  Lu M, Wingfield MJ, Gillette NE, Mori SR, Sun JH (2010) Complex interactions among host pines and fungi vectored by an invasive bark beetle. New Phytologist 187: 859–866.
[52]  Helms KR, Vinson S (2008) Plant resources and colony growth in an invasive ant: the importance of honeydew-producing hemiptera in carbohydrate transfer across trophic levels. Environmental entomology 37: 487–493.
[53]  Zhou AM, Lu YY, Zeng L, Xu YJ, Liang GW (2012) Effects of honeydew of Phenacoccus solenopsis on foliar foraging by Solenopsis invcta. Sociobiology 59: 71–79.
[54]  Li J, Han SC, Li ZG, Zhang BS (2008) The behavior observes of Tapinoma melanocephalum native competitive species of Solenopsis invicta. Plant Quarantine 22: 19–21.
[55]  Wheeler WM (1960) Ants: their structure, development, and behavior. New York and London: Columbia University Press.
[56]  Eisner T (1957) A comparative morphological study of the proventriculus of ants (Hymenoptera: Formicidae). Bulletin of the Museum of Comparative Zoology 116: 429–490.
[57]  Yao I, Shibao H, Akimoto S (2000) Costs and benefits of ant attendance to the drepanosiphid aphid Tuberculatus quercicola. Oikos 89: 3–10.
[58]  Kaplan I, Eubanks MD (2002) Disruption of cotton aphid (Homoptera: Aphididae) – Natural enemy dynamics by red imported fire ants (Hymenoptera: Formicidae). Environmental entomology 31: 1175–1183.
[59]  Coppler LB, Murphy JF, Eubanks MD (2007) Red imported fire ants (Hymenoptera: Formicidae) increase the abundance of aphids in tomato. Florida Entomologist 90: 419–425.
[60]  Diaz D, Knutson A, Bernal JS (2004) Effect of the red imported fire ant on cotton aphid population density and predation of bollworm and beet armyworm eggs. Journal of Economic Entomology 97: 222–229.
[61]  Phillips P, Sherk C (1991) To control mealybugs, stop honeydew-seeking ants. California Agriculture 45: 26–28.
[62]  Daane KM, Sime KR, Hogg BN, Bianchi ML, Cooper ML, et al. (2006) Effects of liquid insecticide baits on Argentine ants in California's coastal vineyards. Crop Protection 25: 592–603.
[63]  Daane KM, Sime KR, Fallon J, Cooper ML (2007) Impacts of Argentine ants on mealybugs and their natural enemies in California's coastal vineyards. Ecological Entomology 32: 583–596.
[64]  Stadler B, Dixon AFG, Kindlmann P (2002) Relative fitness of aphids: effects of plant quality and ants. Ecology Letters 5: 216–222.


comments powered by Disqus